Eriksson, Maria E - Circadian Clock Function and its Importance for the Regulation of Growth

Research

Black and white image of Maria Eriksson leaning against a tree trunk

Photo: Happy Wilder

The focus of the research group is to understand the functional aspects of the circadian clockwork in Arabidopsis and trees (Populus and other species), and how this timing machinery regulates growth. To anticipate the diurnal cycle of light and dark during a day and to anticipate the seasonal changes, most organisms have developed a molecular time measuring system called a circadian (from "circa diem" which in Latin means "about a day") oscillator or clock.

Light and temperature can be received by multiple photoreceptors in the red, far-red and blue spectra and mediates re-setting of this clock. In Arabidopsis, there are five red/far-red light photoreceptors called phytochromes (phy). The best characterized are phyA (far-red) and phyB (red). In the blue wavelengths, receptors like the cryptochromes (cry1 and cry2) are important, but also the ZEITLUPE (ZTL) gene family of F-box, Kelch-, and LOV/PAS domain containing proteins are capable of receiving blue light directly to regulate the circadian clock and seasonal timing. A central loop includes the morning expressed CIRCADIAN CLOCK ASSOCIATED1 (CCA1), and LATE ELONGATED HYPOCOTYL (LHY) which are MYB transcription factors that negatively regulate the gene expression of TIMING OF CAB2 EXPRESSION 1 (TOC1) so that it is expressed in the evening when CCA1 and LHY are turned over. TOC1 in turn mitigate expression of CCA1 and LHY. In addition, this negative feedback loop is intertwined with at least two additional interlocked feedback loops.

Populus orthologues of core clock genes LATE ELONGATED 1 (LHY1), LHY2 and TOC1 were targeted by RNA interference (RNAi) and allowed us to experimentally test their clock function and effect on growth. These studies showed that the circadian clock of Populus sp. trees contain a negative feedback loop of LHY1, LHY2 with TOC1 – similar to the situation in Arabidopsis. Our Populus ‘clock mutant’ RNAi trees also helped us to show that these proteins control seasonal timing of growth, cold response and freezing tolerance of trees.

Collage of four photos of the top of a poplar tree showing different growth stages

Figure 1: Signs of season. An apex of Populus in active growth (upper left), at bud set (upper right), during dormancy (lower right) and at bud burst (lower left)

In the daily context, we found that a functional clock and the expression of the morning clock genes LHY1 and LHY2 are needed for growth. A key aspect of their regulation is obtained through regulation of CYCLIN D3 expression and thereby the G1 to S-phase transition of the cell cycle. Their functions are also needed to maintain cytokinin levels required for cell proliferation and growth, promoting biomass of plants.

Our very recent work places the photoreceptor and circadian clock protein ZTL (introduced above) as a critical integrator of light and circadian clock function with abscisic acid (ABA) signalling. ZTL promotes ABA-induced stomatal closure. It acts upstream of the PSEUDO-RESPONSE REGULATOR 5 (PRR5) to mitigate its function – but in addition ZTL also promotes ABA-induced gene expression and partner up with OPEN STOMATA 1 (OST1) to induce closing of stomata in response to ABA under drought stress. While timely expression of PRRs from dawn till dusk help keep stomata open, ZTL can short-cut and promote closure at the right time of day and in time of stress. Further, the role of ZTL is conserved between Arabidopsis and Populus trees. This picture (below) summarises our recent findings by Jurca et al., (2022).

Schematic overview on how ZEITLUPE promotes ABA regulated stomata closure

Figure 2: Wild type (WT) and zeitlupe (ztl) mutants in Arabidopsis and Populus sp. trees show different responses to applied stress hormone abscisic acid (ABA) or drought stress in midday. The difference is for instance manifested by the inability of ztl mutants to close stomata to maintain water status in leaves that are detached. Leaves were weighted at regular intervals to track the loss of water vapor through stomata and those experiments showed a much larger water loss from the ztl mutant (shown by large water droplets in the picture) compared to the WT (smaller water droplets) in our recently published study by Jurca et al., 2022 in Frontiers in Plant Science. We also tested another clock mutant with a deficiency in PSUEDO-RESPONSE REGULATOR 5 (PRR5) (the prr5-1 mutant) which showed that PRR5 mitigates closure of stomata. The latter was elucidated using a triple mutant of ztl-3, prr5-1 and open stomata 1-3 (ost1-3). Our results suggested that ZTL could act to inhibit PRR5 (plain T-formed bar shows inhibition of activity, dotted bars indicate loss of this function) as well as independently to promote (plain arrow shows positive action, dotted arrows show loss-of-function) stomatal closure at the right time, in response to ABA and stress to protect the plant from losing precious water. (Illustration made by DC SciArt)

Hence, as we learn more about temporal regulation, there is a great potential for biotechnological application in adapting new plants or re-adapting (in case of climate warming) local plants to rapidly evolving "new" local conditions. Such adaptation may involve a means to increase the length of critical daylength requirements of plants to match a novel growth season, while keeping winter hardiness, as well as increasing biomass production.

To experimentally explore clock function and its role in growth, we use Arabidopsis thaliana for gene discovery. As tree model systems, we mainly use the deciduous tree hybrid aspen (Populus tremula x P. tremuloides) and the gymnosperm Norway spruce (Picea abies) to address the clock’s role in wood regulation and growth. We apply forward and reverse genetic approaches as well as assays of natural variation, as appropriate.

In the laboratory, we also use a combination of bioinformatics, genetic and molecular tools with in vitro/in vivo studies to study clock and protein function. Such tools for studying the clockwork and its adaptive value include plant cells or plants with altered levels of clock gene expression, molecular tools such as RNAseq, promoter:LUCIFERASE expression, real time PCR and protein assays to monitor circadian clock regulated gene and protein expression. To investigate perennial growth, we monitor elongation and diameter growth as well as physiological manifestations of season such as flowering, growth cessation, bud set and bud break. Mutants with an altered timing mechanism in this way help us to build a model for clock function and its impact on daily and seasonal regulation of growth.

Tips of populus trees in pixalated blue-to-white or green-to-yellow colour.

Figure 3: Populus trees carrying firefly LUCIFERASE under control of a circadianly controlled promoter

Together, our studies of the circadian clock have contributed to understanding the importance of the circadian clock mechanism in weeds and trees: from its crucial impact on controlling water balance and photosynthesis through the control of stomatal regulation, to metabolism and synthesis of plant hormones as well as regulation of the cell cycle. Our future studies will further clarify the circadian clock mechanism and the important aspects of daily and seasonal timing for plant growth and development.

Key Publications

Jurca, M., Sjölander, J., Ibáñez, C., Matrosova, A., Johansson, M., Kozarewa, I., Takata, N., Bakó, L., Webb, A. A. R., Israelsson-Nordström, M., & Eriksson, M. E. (2022) ZEITLUPE Promotes ABA-Induced Stomatal Closure in Arabidopsis and Populus. Frontiers in Plant Science https://doi.org/10.3389/fpls.2022.829121
Edwards KD, Takata N, Johansson M, Jurca M, Novák O, Hényková E, Liverani S, Kozarewa I, Strnad M, Millar AJ, Ljung K, Eriksson ME (2018) Circadian clock components control daily growth activities by modulating cytokinin levels and cell division-associated gene expression in Populus trees. Plant Cell & Environment: 41(6):1468-1482 https://doi.org/10.1111/pce.13185
Eriksson, M. E., Hoffman, D., Kaduk, M., Mauriat, M., & Moritz, T. (2015) Transgenic hybrid aspen trees with increased gibberellin (GA) concentrations suggest that GA acts in parallel with FLOWERING LOCUS T2 to control shoot elongation. New Phytologist, 205(3): 1288–1295. https://nph.onlinelibrary.wiley.com/doi/pdf/10.1111/nph.13144
Johansson M, McWatters HG, Bakó L, Takata N, Gyula P, Hall A, Somers DE, Millar AJ, Eriksson ME (2011). Partners in time: EARLY BIRD associates with ZEITLUPE and regulates the speed of the Arabidopsis clock. Plant Physiology: 155:2108-2122 https://doi.org/10.1104/pp.110.167155
Ashelford K, Eriksson ME, Allen CM, D’Amore L, Johansson M, Gould P, Kay S, Millar AJ, Hall N, Hall A (2011). Full genome re-sequencing reveals a novel circadian clock mutation in Arabidopsis. Genome Biology: 12:R28, 12 pp https://doi.org/10.1186/gb-2011-12-3-r28
Ibáñez C, Kozarewa I, Johansson M, Ögren E, Rohde A, Eriksson ME (2010). Circadian clock components regulate entry and affect exit of seasonal dormancy as well as winter hardiness in Populus trees. Plant Physiology: 153:1823-1833 https://doi.org/10.1104/pp.110.158220
Kozarewa I, Ibáñez C, Johansson M, Ögren E, Mozley D, Nylander E, Chono M, Moritz T, Eriksson ME (2010). Alteration of PHYA expression change circadian rhythms and timing of bud set in Populus. Plant Molecular Biology: 73:143-156 https://doi.org/10.1007/s11103-010-9619-2
Eriksson ME, Hanano S, Southern MM, Hall A, Millar AJ (2003). Response regulator homologues have complementary, light- dependent functions in the Arabidopsis circadian clock. Planta: 218:159-162 https://doi.org/10.1007/s00425-003-1106-4
Eriksson ME, Israelsson M, Olsson O, Moritz T (2000). Increased gibberellin biosynthesis in transgenic trees promotes growth, biomass production and xylem fiber length. Nature Biotechnology 18:784-788 https://doi.org/10.1038/77355

Publications

BibBase eriksson, m

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2022 (3)

Monitoring Seasonal Bud Set, Bud Burst, and Cold Hardiness in Populus. Johansson, M., Takata, N., Ibáñez, C., & Eriksson, M. E. In Staiger, D., Davis, S., & Davis, A. M., editor(s), Plant Circadian Networks: Methods and Protocols, of Methods in Molecular Biology, pages 215–226. Springer US, New York, NY, January 2022.

Monitoring Seasonal Bud Set, Bud Burst, and Cold Hardiness in Populus [link]

Paper link bibtex abstract

@incollection{johansson_monitoring_2022,
	address = {New York, NY},
	series = {Methods in {Molecular} {Biology}},
	title = {Monitoring {Seasonal} {Bud} {Set}, {Bud} {Burst}, and {Cold} {Hardiness} in {Populus}},
	isbn = {978-1-07-161912-4},
	url = {https://doi.org/10.1007/978-1-0716-1912-4_17},
	abstract = {Using a perennial model plant allows the study of reoccurring seasonal events in a way that is not possible using a fast-growing annual such as A. thaliana (Arabidopsis). In this study, we present a hybrid aspen (Populus tremula × P. tremuloides) as our perennial model plant. These plants can be grown in growth chambers to shorten growth periods and manipulate day length and temperature in ways that would be impossible under natural conditions. In addition, the use of growth chambers allows easy monitoring of height and diameter expansion, accelerating the collection of data from new strategies that allow evaluation of promoters or inhibitors of growth. Here, we describe how to study and quantify responses to seasonal changes (mainly using P. tremula × P. tremuloides) by measuring growth rate and key events under different photoperiodic cycles.},
	language = {en},
	urldate = {2021-12-01},
	booktitle = {Plant {Circadian} {Networks}: {Methods} and {Protocols}},
	publisher = {Springer US},
	author = {Johansson, Mikael and Takata, Naoki and Ibáñez, Cristian and Eriksson, Maria E.},
	editor = {Staiger, Dorothee and Davis, Seth and Davis, Amanda Melaragno},
	month = jan,
	year = {2022},
	keywords = {Bud burst, Bud set, Cold acclimation, Critical day length, Freezing tolerance, Perennial, Photoperiod, Populus},
	pages = {215--226},
}

The Perennial Clock Is an Essential Timer for Seasonal Growth Events and Cold Hardiness. Johansson, M., Ibáñez, C., Takata, N., & Eriksson, M. E. In Staiger, D., Davis, S., & Davis, A. M., editor(s), Plant Circadian Networks: Methods and Protocols, of Methods in Molecular Biology, pages 227–242. Springer US, New York, NY, January 2022.

Paper link bibtex abstract

@incollection{johansson_perennial_2022,
	address = {New York, NY},
	series = {Methods in {Molecular} {Biology}},
	title = {The {Perennial} {Clock} {Is} an {Essential} {Timer} for {Seasonal} {Growth} {Events} and {Cold} {Hardiness}},
	isbn = {978-1-07-161912-4},
	url = {https://doi.org/10.1007/978-1-0716-1912-4_18},
	abstract = {Over the last several decades, changes in global temperatures have led to changes in local environments affecting the growth conditions for many species. This is a trend that makes it even more important to understand how plants respond to local variations and seasonal changes in climate.To detect daily and seasonal changes as well as acute stress factors such as cold and drought, plants rely on a circadian clock. This chapter introduces the current knowledge and literature about the setup and function of the circadian clock in various tree and perennial species, with a focus on the Populus genus.},
	language = {en},
	urldate = {2021-12-01},
	booktitle = {Plant {Circadian} {Networks}: {Methods} and {Protocols}},
	publisher = {Springer US},
	author = {Johansson, Mikael and Ibáñez, Cristian and Takata, Naoki and Eriksson, Maria E.},
	editor = {Staiger, Dorothee and Davis, Seth and Davis, Amanda Melaragno},
	month = jan,
	year = {2022},
	keywords = {Bud burst, Bud set, Circadian clock, Cold tolerance, Growth, Perennial plants, Populus, Seasonal regulation},
	pages = {227--242},
}

ZEITLUPE Promotes ABA-Induced Stomatal Closure in Arabidopsis and Populus. Jurca, M., Sjölander, J., Ibáñez, C., Matrosova, A., Johansson, M., Kozarewa, I., Takata, N., Bakó, L., Webb, A. A. R., Israelsson-Nordström, M., & Eriksson, M. E. Frontiers in Plant Science, 13. March 2022.

ZEITLUPE Promotes ABA-Induced Stomatal Closure in Arabidopsis and Populus [link]

Paper link bibtex abstract

@article{jurca_zeitlupe_2022,
	title = {{ZEITLUPE} {Promotes} {ABA}-{Induced} {Stomatal} {Closure} in {Arabidopsis} and {Populus}},
	volume = {13},
	issn = {1664-462X},
	url = {https://www.frontiersin.org/article/10.3389/fpls.2022.829121},
	abstract = {Plants balance water availability with gas exchange and photosynthesis by controlling stomatal aperture. This control is regulated in part by the circadian clock, but it remains unclear how signalling pathways of daily rhythms are integrated into stress responses. The serine/threonine protein kinase OPEN STOMATA 1 (OST1) contributes to the regulation of stomatal closure via activation of S-type anion channels. OST1 also mediates gene regulation in response to ABA/drought stress. We show that ZEITLUPE (ZTL), a blue light photoreceptor and clock component, also regulates ABA-induced stomatal closure in Arabidopsis thaliana, establishing a link between clock and ABA-signalling pathways. ZTL sustains expression of OST1 and ABA-signalling genes. Stomatal closure in response to ABA is reduced in ztl mutants, which maintain wider stomatal apertures and show higher rates of gas exchange and water loss than wild-type plants. Detached rosette leaf assays revealed a stronger water loss phenotype in ztl-3, ost1-3 double mutants, indicating that ZTL and OST1 contributed synergistically to the control of stomatal aperture. Experimental studies of Populus sp., revealed that ZTL regulated the circadian clock and stomata, indicating ZTL function was similar in these trees and Arabidopsis. PSEUDO-RESPONSE REGULATOR 5 (PRR5), a known target of ZTL, affects ABA-induced responses, including stomatal regulation. Like ZTL, PRR5 interacted physically with OST1 and contributed to the integration of ABA responses with circadian clock signalling. This suggests a novel mechanism whereby the PRR proteins—which are expressed from dawn to dusk—interact with OST1 to mediate ABA-dependent plant responses to reduce water loss in time of stress.},
	urldate = {2022-03-02},
	journal = {Frontiers in Plant Science},
	author = {Jurca, Manuela and Sjölander, Johan and Ibáñez, Cristian and Matrosova, Anastasia and Johansson, Mikael and Kozarewa, Iwanka and Takata, Naoki and Bakó, Laszlo and Webb, Alex A. R. and Israelsson-Nordström, Maria and Eriksson, Maria E.},
	month = mar,
	year = {2022},
	keywords = {⛔ No DOI found},
}

2021 (1)

Growing in time: exploring the molecular mechanisms of tree growth. Singh, R. K., Bhalerao, R. P., & Eriksson, M. E. Tree Physiology, 41(4): 657–678. April 2021.

Growing in time: exploring the molecular mechanisms of tree growth [link]

Paper doi link bibtex abstract

@article{singh_growing_2021,
	title = {Growing in time: exploring the molecular mechanisms of tree growth},
	volume = {41},
	issn = {1758-4469},
	shorttitle = {Growing in time},
	url = {https://academic.oup.com/treephys/article/41/4/657/5848548},
	doi = {10.1093/treephys/tpaa065},
	abstract = {Abstract
            Trees cover vast areas of the Earth’s landmasses. They mitigate erosion, capture carbon dioxide, produce oxygen and support biodiversity, and also are a source of food, raw materials and energy for human populations. Understanding the growth cycles of trees is fundamental for many areas of research. Trees, like most other organisms, have evolved a circadian clock to synchronize their growth and development with the daily and seasonal cycles of the environment. These regular changes in light, daylength and temperature are perceived via a range of dedicated receptors and cause resetting of the circadian clock to local time. This allows anticipation of daily and seasonal fluctuations and enables trees to co-ordinate their metabolism and physiology to ensure vital processes occur at the optimal times. In this review, we explore the current state of knowledge concerning the regulation of growth and seasonal dormancy in trees, using information drawn from model systems such as Populus spp.},
	language = {en},
	number = {4},
	urldate = {2021-06-07},
	journal = {Tree Physiology},
	author = {Singh, Rajesh Kumar and Bhalerao, Rishikesh P. and Eriksson, Maria E.},
	editor = {Polle, Andrea},
	month = apr,
	year = {2021},
	pages = {657--678},
}

2020 (1)

Current status of the multinational Arabidopsis community. Parry, G., Provart, N. J., Brady, S. M., Uzilday, B., & Committee, T. M. A. S. Plant Direct, 4(7): e00248. 2020. _eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1002/pld3.248

Current status of the multinational Arabidopsis community [link]

Paper doi link bibtex abstract

@article{parry_current_2020,
	title = {Current status of the multinational {Arabidopsis} community},
	volume = {4},
	issn = {2475-4455},
	url = {https://onlinelibrary.wiley.com/doi/abs/10.1002/pld3.248},
	doi = {10/gpn668},
	abstract = {The multinational Arabidopsis research community is highly collaborative and over the past thirty years these activities have been documented by the Multinational Arabidopsis Steering Committee (MASC). Here, we (a) highlight recent research advances made with the reference plant Arabidopsis thaliana; (b) provide summaries from recent reports submitted by MASC subcommittees, projects and resources associated with MASC and from MASC country representatives; and (c) initiate a call for ideas and foci for the “fourth decadal roadmap,” which will advise and coordinate the global activities of the Arabidopsis research community.},
	language = {en},
	number = {7},
	urldate = {2022-03-14},
	journal = {Plant Direct},
	author = {Parry, Geraint and Provart, Nicholas J. and Brady, Siobhan M. and Uzilday, Baris and Committee, The Multinational Arabidopsis Steering},
	year = {2020},
	note = {\_eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1002/pld3.248},
	keywords = {Arabidopsis thaliana, Research Network, collaboration, roadmap},
	pages = {e00248},
}

2018 (3)

Autumn senescence in aspen is not triggered by day length. Michelson, I. H., Ingvarsson, P. K., Robinson, K. M., Edlund, E., Eriksson, M. E., Nilsson, O., & Jansson, S. Physiologia Plantarum, 162(1): 123–134. January 2018.

Autumn senescence in aspen is not triggered by day length [link]

Paper doi link bibtex

@article{michelson_autumn_2018,
	title = {Autumn senescence in aspen is not triggered by day length},
	volume = {162},
	issn = {00319317},
	url = {http://doi.wiley.com/10.1111/ppl.12593},
	doi = {10.1111/ppl.12593},
	language = {en},
	number = {1},
	urldate = {2021-06-07},
	journal = {Physiologia Plantarum},
	author = {Michelson, Ingrid H. and Ingvarsson, Pär K. and Robinson, Kathryn M. and Edlund, Erik and Eriksson, Maria E. and Nilsson, Ove and Jansson, Stefan},
	month = jan,
	year = {2018},
	pages = {123--134},
}

Circadian clock components control daily growth activities by modulating cytokinin levels and cell division-associated gene expression in Populus trees: Control of growth in Populus. Edwards, K. D., Takata, N., Johansson, M., Jurca, M., Novák, O., Hényková, E., Liverani, S., Kozarewa, I., Strnad, M., Millar, A. J., Ljung, K., & Eriksson, M. E. Plant, Cell & Environment, 41(6): 1468–1482. June 2018.

Paper doi link bibtex

@article{edwards_circadian_2018,
	title = {Circadian clock components control daily growth activities by modulating cytokinin levels and cell division-associated gene expression in \textit{{Populus}} trees: {Control} of growth in {Populus}.},
	volume = {41},
	issn = {01407791},
	shorttitle = {Circadian clock components control daily growth activities by modulating cytokinin levels and cell division-associated gene expression in \textit{{Populus}} trees},
	url = {http://doi.wiley.com/10.1111/pce.13185},
	doi = {10/gd8xdq},
	language = {en},
	number = {6},
	urldate = {2021-06-07},
	journal = {Plant, Cell \& Environment},
	author = {Edwards, Kieron D. and Takata, Naoki and Johansson, Mikael and Jurca, Manuela and Novák, Ondřej and Hényková, Eva and Liverani, Silvia and Kozarewa, Iwanka and Strnad, Miroslav and Millar, Andrew J. and Ljung, Karin and Eriksson, Maria E.},
	month = jun,
	year = {2018},
	pages = {1468--1482},
}

GIGANTEA-like genes control seasonal growth cessation in Populus. Ding, J., Böhlenius, H., Rühl, M. G., Chen, P., Sane, S., Zambrano, J. A., Zheng, B., Eriksson, M. E., & Nilsson, O. New Phytologist, 218(4): 1491–1503. 2018. _eprint: https://nph.onlinelibrary.wiley.com/doi/pdf/10.1111/nph.15087

GIGANTEA-like genes control seasonal growth cessation in Populus [link]

Paper doi link bibtex abstract

@article{ding_gigantea-like_2018,
	title = {{GIGANTEA}-like genes control seasonal growth cessation in {Populus}},
	volume = {218},
	copyright = {© 2018 The Authors. New Phytologist © 2018 New Phytologist Trust},
	issn = {1469-8137},
	url = {https://nph.onlinelibrary.wiley.com/doi/abs/10.1111/nph.15087},
	doi = {10/gdt24k},
	abstract = {Survival of trees growing in temperate zones requires cycling between active growth and dormancy. This involves growth cessation in the autumn triggered by a photoperiod shorter than the critical day length. Variations in GIGANTEA (GI)-like genes have been associated with phenology in a range of different tree species, but characterization of the functions of these genes in the process is still lacking. We describe the identification of the Populus orthologs of GI and their critical role in short-day-induced growth cessation. Using ectopic expression and silencing, gene expression analysis, protein interaction and chromatin immunoprecipitation experiments, we show that PttGIs are likely to act in a complex with PttFKF1s (FLAVIN-BINDING, KELCH REPEAT, F-BOX 1) and PttCDFs (CYCLING DOF FACTOR) to control the expression of PttFT2, the key gene regulating short-day-induced growth cessation in Populus. In contrast to Arabidopsis, in which the GI-CONSTANS (CO)-FLOWERING LOCUS T (FT) regulon is a crucial day-length sensor for flowering time, our study suggests that, in Populus, PttCO-independent regulation of PttFT2 by PttGI is more important in the photoperiodic control of growth cessation and bud set.},
	language = {en},
	number = {4},
	urldate = {2021-06-21},
	journal = {New Phytologist},
	author = {Ding, Jihua and Böhlenius, Henrik and Rühl, Mark Georg and Chen, Peng and Sane, Shashank and Zambrano, Jose A. and Zheng, Bo and Eriksson, Maria E. and Nilsson, Ove},
	year = {2018},
	note = {\_eprint: https://nph.onlinelibrary.wiley.com/doi/pdf/10.1111/nph.15087},
	keywords = {FLOWERING LOCUS (FT), GIGANTEA (GI), Populus, growth cessation, photoperiod},
	pages = {1491--1503},
}

2016 (3)

Circadian and Plastid Signaling Pathways Are Integrated to Ensure Correct Expression of the CBF and COR Genes during Photoperiodic Growth. Norén, L., Kindgren, P., Stachula, P., Rühl, M., Eriksson, M. E., Hurry, V., & Strand, Å. Plant Physiology, 171(2): 1392–1406. June 2016.

Circadian and Plastid Signaling Pathways Are Integrated to Ensure Correct Expression of the CBF and COR Genes during Photoperiodic Growth [link]

Paper doi link bibtex abstract

@article{noren_circadian_2016,
	title = {Circadian and {Plastid} {Signaling} {Pathways} {Are} {Integrated} to {Ensure} {Correct} {Expression} of the {CBF} and {COR} {Genes} during {Photoperiodic} {Growth}},
	volume = {171},
	issn = {0032-0889},
	url = {https://doi.org/10.1104/pp.16.00374},
	doi = {10/f3rvjv},
	abstract = {The circadian clock synchronizes a wide range of biological processes with the day/night cycle, and correct circadian regulation is essential for photosynthetic activity and plant growth. We describe here a mechanism where a plastid signal converges with the circadian clock to fine-tune the regulation of nuclear gene expression in Arabidopsis (Arabidopsis thaliana). Diurnal oscillations of tetrapyrrole levels in the chloroplasts contribute to the regulation of the nucleus-encoded transcription factors C-REPEAT BINDING FACTORS (CBFs). The plastid signal triggered by tetrapyrrole accumulation inhibits the activity of cytosolic HEAT SHOCK PROTEIN90 and, as a consequence, the maturation and stability of the clock component ZEITLUPE (ZTL). ZTL negatively regulates the transcription factor LONG HYPOCOTYL5 (HY5) and PSEUDO-RESPONSE REGULATOR5 (PRR5). Thus, low levels of ZTL result in a HY5- and PRR5-mediated repression of CBF3 and PRR5-mediated repression of CBF1 and CBF2 expression. The plastid signal thereby contributes to the rhythm of CBF expression and the downstream COLD RESPONSIVE expression during day/night cycles. These findings provide insight into how plastid signals converge with, and impact upon, the activity of well-defined clock components involved in circadian regulation.},
	number = {2},
	urldate = {2021-06-07},
	journal = {Plant Physiology},
	author = {Norén, Louise and Kindgren, Peter and Stachula, Paulina and Rühl, Mark and Eriksson, Maria E. and Hurry, Vaughan and Strand, Åsa},
	month = jun,
	year = {2016},
	pages = {1392--1406},
}

HSP90, ZTL, PRR5 and HY5 integrate circadian and plastid signaling pathways to regulate CBF and COR expression. Noren, L., Kindgren, P., Stachula, P., Ruhl, M., Eriksson, M. E., Hurry, V., & Strand, A. Plant Physiology,pp.00374.2016. April 2016.

HSP90, ZTL, PRR5 and HY5 integrate circadian and plastid signaling pathways to regulate CBF and COR expression. [link]

Paper doi link bibtex

@article{noren_hsp90_2016,
	title = {{HSP90}, {ZTL}, {PRR5} and {HY5} integrate circadian and plastid signaling pathways to regulate {CBF} and {COR} expression.},
	issn = {0032-0889, 1532-2548},
	url = {https://academic.oup.com/plphys/article/171/2/1392-1406/6115310},
	doi = {10/f3rvjv},
	language = {en},
	urldate = {2021-06-07},
	journal = {Plant Physiology},
	author = {Noren, Louise and Kindgren, Peter and Stachula, Paulina and Ruhl, Mark and Eriksson, Maria E. and Hurry, Vaughan and Strand, Asa},
	month = apr,
	year = {2016},
	pages = {pp.00374.2016},
}

Plant Circadian Rhythms. McWatters, H. G, & Eriksson, M. E. In John Wiley & Sons Ltd, editor(s), eLS, pages 1–10. John Wiley & Sons, Ltd, Chichester, UK, May 2016.

Paper doi link bibtex

@incollection{john_wiley__sons_ltd_plant_2016,
	address = {Chichester, UK},
	title = {Plant {Circadian} {Rhythms}},
	isbn = {978-0-470-01590-2 978-0-470-01617-6},
	url = {http://doi.wiley.com/10.1002/9780470015902.a0020113.pub2},
	language = {en},
	urldate = {2021-06-07},
	booktitle = {{eLS}},
	publisher = {John Wiley \& Sons, Ltd},
	author = {McWatters, Harriet G and Eriksson, Maria E.},
	editor = {{John Wiley \& Sons Ltd}},
	month = may,
	year = {2016},
	doi = {10.1002/9780470015902.a0020113.pub2},
	pages = {1--10},
}

2015 (2)

Role of the Circadian Clock in Cold Acclimation and Winter Dormancy in Perennial Plants. Johansson, M., Ramos-Sánchez, J. M., Conde, D., Ibáñez, C., Takata, N., Allona, I., & Eriksson, M. E. In Anderson, J. V., editor(s), Advances in Plant Dormancy, pages 51–74. Springer International Publishing, Cham, 2015.

Paper doi link bibtex

@incollection{anderson_role_2015,
	address = {Cham},
	title = {Role of the {Circadian} {Clock} in {Cold} {Acclimation} and {Winter} {Dormancy} in {Perennial} {Plants}},
	isbn = {978-3-319-14450-4 978-3-319-14451-1},
	url = {http://link.springer.com/10.1007/978-3-319-14451-1_3},
	language = {en},
	urldate = {2021-06-07},
	booktitle = {Advances in {Plant} {Dormancy}},
	publisher = {Springer International Publishing},
	author = {Johansson, Mikael and Ramos-Sánchez, José M. and Conde, Daniel and Ibáñez, Cristian and Takata, Naoki and Allona, Isabel and Eriksson, Maria E.},
	editor = {Anderson, James V.},
	year = {2015},
	doi = {10.1007/978-3-319-14451-1_3},
	pages = {51--74},
}

Transgenic hybrid aspen trees with increased gibberellin (GA) concentrations suggest that GA acts in parallel with FLOWERING LOCUS T2 to control shoot elongation. Eriksson, M. E., Hoffman, D., Kaduk, M., Mauriat, M., & Moritz, T. New Phytologist, 205(3): 1288–1295. 2015. _eprint: https://nph.onlinelibrary.wiley.com/doi/pdf/10.1111/nph.13144

Paper doi link bibtex abstract

@article{eriksson_transgenic_2015,
	title = {Transgenic hybrid aspen trees with increased gibberellin ({GA}) concentrations suggest that {GA} acts in parallel with {FLOWERING} {LOCUS} {T2} to control shoot elongation},
	volume = {205},
	issn = {1469-8137},
	url = {https://nph.onlinelibrary.wiley.com/doi/abs/10.1111/nph.13144},
	doi = {10/f3nxc2},
	abstract = {Bioactive gibberellins (GAs) have been implicated in short day (SD)-induced growth cessation in Populus, because exogenous applications of bioactive GAs to hybrid aspens (Populus tremula × tremuloides) under SD conditions delay growth cessation. However, this effect diminishes with time, suggesting that plants may cease growth following exposure to SDs due to a reduction in sensitivity to GAs. In order to validate and further explore the role of GAs in growth cessation, we perturbed GA biosynthesis or signalling in hybrid aspen plants by overexpressing AtGA20ox1, AtGA2ox2 and PttGID1.3 (encoding GA biosynthesis enzymes and a GA receptor). We found trees with elevated concentrations of bioactive GA, due to overexpression of AtGA20ox1, continued to grow in SD conditions and were insensitive to the level of FLOWERING LOCUS T2 (FT2) expression. As transgenic plants overexpressing the PttGID1.3 GA receptor responded in a wild-type (WT) manner to SD conditions, this insensitivity did not result from limited receptor availability. As high concentrations of bioactive GA during SD conditions were sufficient to sustain shoot elongation growth in hybrid aspen trees, independent of FT2 expression levels, we conclude elongation growth in trees is regulated by both GA- and long day-responsive pathways, similar to the regulation of flowering in Arabidopsis thaliana.},
	language = {en},
	number = {3},
	urldate = {2021-08-31},
	journal = {New Phytologist},
	author = {Eriksson, Maria E. and Hoffman, Daniel and Kaduk, Mateusz and Mauriat, Mélanie and Moritz, Thomas},
	year = {2015},
	note = {\_eprint: https://nph.onlinelibrary.wiley.com/doi/pdf/10.1111/nph.13144},
	keywords = {Flowering Locus T2 (FT2), Populus, gibberellins (GA), growth cessation, photoperiod},
	pages = {1288--1295},
}

2014 (2)

Monitoring Seasonal Bud Set, Bud Burst, and Cold Hardiness in Populus. Johansson, M., Takata, N., Ibáñez, C., & Eriksson, M. E. In Staiger, D., editor(s), Plant Circadian Networks, volume 1158, pages 313–324. Springer New York, New York, NY, 2014. Series Title: Methods in Molecular Biology

Paper doi link bibtex

@incollection{staiger_monitoring_2014,
	address = {New York, NY},
	title = {Monitoring {Seasonal} {Bud} {Set}, {Bud} {Burst}, and {Cold} {Hardiness} in {Populus}},
	volume = {1158},
	isbn = {978-1-4939-0699-4 978-1-4939-0700-7},
	url = {http://link.springer.com/10.1007/978-1-4939-0700-7_21},
	urldate = {2021-06-08},
	booktitle = {Plant {Circadian} {Networks}},
	publisher = {Springer New York},
	author = {Johansson, Mikael and Takata, Naoki and Ibáñez, Cristian and Eriksson, Maria E.},
	editor = {Staiger, Dorothee},
	year = {2014},
	doi = {10.1007/978-1-4939-0700-7_21},
	note = {Series Title: Methods in Molecular Biology},
	pages = {313--324},
}

The Perennial Clock Is an Essential Timer for Seasonal Growth Events and Cold Hardiness. Johansson, M., Ibáñez, C., Takata, N., & Eriksson, M. E. In Staiger, D., editor(s), Plant Circadian Networks, volume 1158, pages 297–311. Springer New York, New York, NY, 2014. Series Title: Methods in Molecular Biology

Paper doi link bibtex

@incollection{staiger_perennial_2014,
	address = {New York, NY},
	title = {The {Perennial} {Clock} {Is} an {Essential} {Timer} for {Seasonal} {Growth} {Events} and {Cold} {Hardiness}},
	volume = {1158},
	isbn = {978-1-4939-0699-4 978-1-4939-0700-7},
	url = {http://link.springer.com/10.1007/978-1-4939-0700-7_20},
	urldate = {2021-06-08},
	booktitle = {Plant {Circadian} {Networks}},
	publisher = {Springer New York},
	author = {Johansson, Mikael and Ibáñez, Cristian and Takata, Naoki and Eriksson, Maria E.},
	editor = {Staiger, Dorothee},
	year = {2014},
	doi = {10.1007/978-1-4939-0700-7_20},
	note = {Series Title: Methods in Molecular Biology},
	pages = {297--311},
}

2012 (2)

A simple and efficient transient transformation for hybrid aspen (Populus tremula × P. tremuloides). Takata, N., & Eriksson, M. E. Plant Methods, 8(1): 30. 2012.

A simple and efficient transient transformation for hybrid aspen (Populus tremula × P. tremuloides) [link]

Paper doi link bibtex

@article{takata_simple_2012,
	title = {A simple and efficient transient transformation for hybrid aspen ({Populus} tremula × {P}. tremuloides)},
	volume = {8},
	issn = {1746-4811},
	url = {http://plantmethods.biomedcentral.com/articles/10.1186/1746-4811-8-30},
	doi = {10/f236z7},
	language = {en},
	number = {1},
	urldate = {2021-06-08},
	journal = {Plant Methods},
	author = {Takata, Naoki and Eriksson, Maria E.},
	year = {2012},
	pages = {30},
}

The dynamic nature of bud dormancy in trees: environmental control and molecular mechanisms: Bud dormancy in trees. Cooke, J. E. K., Eriksson, M. E., & Junttila, O. Plant, Cell & Environment, 35(10): 1707–1728. October 2012.

The dynamic nature of bud dormancy in trees: environmental control and molecular mechanisms: Bud dormancy in trees [link]

Paper doi link bibtex

@article{cooke_dynamic_2012,
	title = {The dynamic nature of bud dormancy in trees: environmental control and molecular mechanisms: {Bud} dormancy in trees},
	volume = {35},
	issn = {01407791},
	shorttitle = {The dynamic nature of bud dormancy in trees},
	url = {http://doi.wiley.com/10.1111/j.1365-3040.2012.02552.x},
	doi = {10/f22v73},
	language = {en},
	number = {10},
	urldate = {2021-06-08},
	journal = {Plant, Cell \& Environment},
	author = {Cooke, Janice E. K. and Eriksson, Maria E. and Junttila, Olavi},
	month = oct,
	year = {2012},
	pages = {1707--1728},
}

2011 (3)

Full genome re-sequencing reveals a novel circadian clock mutation in Arabidopsis. Ashelford, K., Eriksson, M. E., Allen, C. M, D'Amore, R., Johansson, M., Gould, P., Kay, S., Millar, A. J, Hall, N., & Hall, A. Genome Biology, 12(3): R28. 2011.

Paper doi link bibtex

@article{ashelford_full_2011,
	title = {Full genome re-sequencing reveals a novel circadian clock mutation in {Arabidopsis}},
	volume = {12},
	issn = {1465-6906},
	url = {http://genomebiology.biomedcentral.com/articles/10.1186/gb-2011-12-3-r28},
	doi = {10/dzpfvk},
	language = {en},
	number = {3},
	urldate = {2021-06-08},
	journal = {Genome Biology},
	author = {Ashelford, Kevin and Eriksson, Maria E. and Allen, Christopher M and D'Amore, Rosalinda and Johansson, Mikael and Gould, Peter and Kay, Suzanne and Millar, Andrew J and Hall, Neil and Hall, Anthony},
	year = {2011},
	pages = {R28},
}

Partners in Time: EARLY BIRD Associates with ZEITLUPE and Regulates the Speed of the Arabidopsis Clock. Johansson, M., McWatters, H. G., Bakó, L., Takata, N., Gyula, P., Hall, A., Somers, D. E., Millar, A. J., & Eriksson, M. E. Plant Physiology, 155(4): 2108–2122. March 2011.

Paper doi link bibtex abstract

@article{johansson_partners_2011,
	title = {Partners in {Time}: {EARLY} {BIRD} {Associates} with {ZEITLUPE} and {Regulates} the {Speed} of the {Arabidopsis} {Clock}},
	volume = {155},
	issn = {1532-2548},
	shorttitle = {Partners in {Time}},
	url = {https://academic.oup.com/plphys/article/155/4/2108/6108867},
	doi = {10/bgh2rc},
	abstract = {Abstract
            The circadian clock of the model plant Arabidopsis (Arabidopsis thaliana) is made up of a complex series of interacting feedback loops whereby proteins regulate their own expression across day and night. early bird (ebi) is a circadian mutation that causes the clock to speed up: ebi plants have short circadian periods, early phase of clock gene expression, and are early flowering. We show that EBI associates with ZEITLUPE (ZTL), known to act in the plant clock as a posttranslational mediator of protein degradation. However, EBI is not degraded by its interaction with ZTL. Instead, ZTL counteracts the effect of EBI during the day and increases it at night, modulating the expression of key circadian components. The partnership of EBI with ZTL reveals a novel mechanism involved in controlling the complex transcription-translation feedback loops of the clock. This work highlights the importance of cross talk between the ubiquitination pathway and transcriptional control for regulation of the plant clock.},
	language = {en},
	number = {4},
	urldate = {2021-06-08},
	journal = {Plant Physiology},
	author = {Johansson, Mikael and McWatters, Harriet G. and Bakó, László and Takata, Naoki and Gyula, Péter and Hall, Anthony and Somers, David E. and Millar, Andrew J. and Eriksson, Maria E.},
	month = mar,
	year = {2011},
	pages = {2108--2122},
}

Plant cell responses to cold are all about timing. Eriksson, M. E., & Webb, A. A. Current Opinion in Plant Biology, 14(6): 731–737. December 2011.

Plant cell responses to cold are all about timing [link]

Paper doi link bibtex

@article{eriksson_plant_2011,
	title = {Plant cell responses to cold are all about timing},
	volume = {14},
	issn = {13695266},
	url = {https://linkinghub.elsevier.com/retrieve/pii/S1369526611001282},
	doi = {10/bwjm2f},
	language = {en},
	number = {6},
	urldate = {2021-06-08},
	journal = {Current Opinion in Plant Biology},
	author = {Eriksson, Maria E. and Webb, Alex AR},
	month = dec,
	year = {2011},
	pages = {731--737},
}

2010 (3)

Alteration of PHYA expression change circadian rhythms and timing of bud set in Populus. Kozarewa, I., Ibáñez, C., Johansson, M., Ögren, E., Mozley, D., Nylander, E., Chono, M., Moritz, T., & Eriksson, M. E. Plant Molecular Biology, 73(1-2): 143–156. May 2010.

Alteration of PHYA expression change circadian rhythms and timing of bud set in Populus [link]

Paper doi link bibtex

@article{kozarewa_alteration_2010,
	title = {Alteration of {PHYA} expression change circadian rhythms and timing of bud set in {Populus}},
	volume = {73},
	issn = {0167-4412, 1573-5028},
	url = {http://link.springer.com/10.1007/s11103-010-9619-2},
	doi = {10/dp553q},
	language = {en},
	number = {1-2},
	urldate = {2021-06-08},
	journal = {Plant Molecular Biology},
	author = {Kozarewa, Iwanka and Ibáñez, Cristian and Johansson, Mikael and Ögren, Erling and Mozley, David and Nylander, Eva and Chono, Makiko and Moritz, Thomas and Eriksson, Maria E.},
	month = may,
	year = {2010},
	pages = {143--156},
}

Changes in diurnal patterns within the Populus transcriptome and metabolome in response to photoperiod variation. Hoffman, D. E., Jonsson, P., Bylesjö, M., Trygg, J., Antti, H., Eriksson, M. E., & Moritz, T. Plant, Cell & Environment, 33(8): 1298–1313. August 2010.
doi link bibtex abstract

@article{hoffman_changes_2010,
	title = {Changes in diurnal patterns within the {Populus} transcriptome and metabolome in response to photoperiod variation},
	volume = {33},
	issn = {1365-3040},
	doi = {10/d2xk8m},
	abstract = {Changes in seasonal photoperiod provides an important environmental signal that affects the timing of winter dormancy in perennial, deciduous, temperate tree species, such as hybrid aspen (Populus tremula x Populus tremuloides). In this species, growth cessation, cold acclimation and dormancy are induced in the autumn by the detection of day-length shortening that occurs at a given critical day length. Important components in the detection of such day-length changes are photoreceptors and the circadian clock, and many plant responses at both the gene regulation and metabolite levels are expected to be diurnal. To directly examine this expectation and study components in these events, here we report transcriptomic and metabolomic responses to a change in photoperiod from long to short days in hybrid aspen. We found about 16\% of genes represented on the arrays to be diurnally regulated, as assessed by our pre-defined criteria. Furthermore, several of these genes were involved in circadian-associated processes, including photosynthesis and primary and secondary metabolism. Metabolites affected by the change in photoperiod were mostly involved in carbon metabolism. Taken together, we have thus established a molecular catalog of events that precede a response to winter.},
	language = {eng},
	number = {8},
	journal = {Plant, Cell \& Environment},
	author = {Hoffman, Daniel E. and Jonsson, Pär and Bylesjö, Max and Trygg, Johan and Antti, Henrik and Eriksson, Maria E. and Moritz, Thomas},
	month = aug,
	year = {2010},
	pmid = {20302601},
	keywords = {Carbohydrate Metabolism, Circadian Rhythm, DNA, Complementary, Gene Expression Profiling, Gene Expression Regulation, Plant, Genes, Plant, Metabolome, Oligonucleotide Array Sequence Analysis, Photoperiod, Populus, Seasons},
	pages = {1298--1313},
}

Circadian Clock Components Regulate Entry and Affect Exit of Seasonal Dormancy as Well as Winter Hardiness in Populus Trees. IbÁñez, C., Kozarewa, I., Johansson, M., Ögren, E., Rohde, A., & Eriksson, M. E. Plant Physiology, 153(4): 1823–1833. August 2010.

Paper doi link bibtex abstract

@article{ibanez_circadian_2010,
	title = {Circadian {Clock} {Components} {Regulate} {Entry} and {Affect} {Exit} of {Seasonal} {Dormancy} as {Well} as {Winter} {Hardiness} in \textit{{Populus}} {Trees}},
	volume = {153},
	issn = {1532-2548},
	url = {https://academic.oup.com/plphys/article/153/4/1823/6111276},
	doi = {10/dzmr76},
	abstract = {Abstract
            This study addresses the role of the circadian clock in the seasonal growth cycle of trees: growth cessation, bud set, freezing tolerance, and bud burst. Populus tremula × Populus tremuloides (Ptt) LATE ELONGATED HYPOCOTYL1 (PttLHY1), PttLHY2, and TIMING OF CAB EXPRESSION1 constitute regulatory clock components because down-regulation by RNA interference of these genes leads to altered phase and period of clock-controlled gene expression as compared to the wild type. Also, both RNA interference lines show about 1-h-shorter critical daylength for growth cessation as compared to the wild type, extending their period of growth. During winter dormancy, when the diurnal variation in clock gene expression stops altogether, down-regulation of PttLHY1 and PttLHY2 expression compromises freezing tolerance and the expression of C-REPEAT BINDING FACTOR1, suggesting a role of these genes in cold hardiness. Moreover, down-regulation of PttLHY1 and PttLHY2 causes a delay in bud burst. This evidence shows that in addition to a role in daylength-controlled processes, PttLHY plays a role in the temperature-dependent processes of dormancy in Populus such as cold hardiness and bud burst.},
	language = {en},
	number = {4},
	urldate = {2021-06-08},
	journal = {Plant Physiology},
	author = {IbÁñez, Cristian and Kozarewa, Iwanka and Johansson, Mikael and Ögren, Erling and Rohde, Antje and Eriksson, Maria E.},
	month = aug,
	year = {2010},
	pages = {1823--1833},
}

2007 (1)

Plant Circadian Rhythms. McWatters, H. G., & Eriksson, M. E. In eLS. American Cancer Society, 2007. _eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1002/9780470015902.a0020113

Paper doi link bibtex abstract

@incollection{mcwatters_plant_2007,
	title = {Plant {Circadian} {Rhythms}},
	copyright = {Copyright © 2007 John Wiley \& Sons, Ltd. All rights reserved.},
	isbn = {978-0-470-01590-2},
	url = {https://onlinelibrary.wiley.com/doi/abs/10.1002/9780470015902.a0020113},
	abstract = {Circadian clocks are found in most eukaryotic organisms. By allowing anticipation of daily and seasonal changes they enable coordination of metabolism and life cycle with the natural rhythms of the environment. Plant circadian rhythms are generated by a series of interlocking feedback loops of ribonucleic acid (RNA) and protein expression that respond to environmental cycles of light and temperature. They control essential processes in the plant's development, such as the transition to flowering or growth cessation.},
	language = {en},
	urldate = {2021-06-10},
	booktitle = {{eLS}},
	publisher = {American Cancer Society},
	author = {McWatters, Harriet G. and Eriksson, Maria E.},
	year = {2007},
	doi = {10.1002/9780470015902.a0020113},
	note = {\_eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1002/9780470015902.a0020113},
	keywords = {Arabidopsis thaliana, Populus, bud set, circadian clock, entrainment, photoperiodism},
}

2006 (1)

Forward genetic analysis of the circadian clock separates the multiple functions of ZEITLUPE. Kevei, E., Gyula, P., Hall, A., Kozma-Bognar, L., Kim, W. Y., Eriksson, M. E., Toth, R., Hanano, S., Feher, B., Southern, M. M., Bastow, R. M., Viczian, A., Hibberd, V., Davis, S. J., Somers, D. E., Nagy, F., & Millar, A. J. Plant Physiology, 140(3): 933–945. March 2006. Place: Rockville Publisher: Amer Soc Plant Biologists WOS:000235868900013
doi link bibtex abstract

@article{kevei_forward_2006,
	title = {Forward genetic analysis of the circadian clock separates the multiple functions of {ZEITLUPE}},
	volume = {140},
	issn = {0032-0889},
	doi = {10/bx2pxd},
	abstract = {The circadian system of Arabidopsis ( Arabidopsis thaliana) includes feedback loops of gene regulation that generate 24-h oscillations. Components of these loops remain to be identified; none of the known components is completely understood, including ZEITLUPE (ZTL), a gene implicated in regulated protein degradation. ztl mutations affect both circadian and developmental responses to red light, possibly through ZTL interaction with PHYTOCHROME B (PHYB). We conducted a large-scale genetic screen that identified additional clock-affecting loci. Other mutants recovered include 11 new ztl alleles encompassing mutations in each of the ZTL protein domains. Each mutation lengthened the circadian period, even in darkgrown seedlings entrained to temperature cycles. A mutation of the LIGHT, OXYGEN, VOLTAGE (LOV)/Period-ARNT-Sim ( PAS) domain was unique in retaining wild-type responses to red light both for the circadian period and for control of hypocotyl elongation. This uncoupling of ztl phenotypes indicates that interactions of ZTL protein with multiple factors must be disrupted to generate the full ztl mutant phenotype. Protein interaction assays showed that the ztl mutant phenotypes were not fully explained by impaired interactions with previously described partner proteins Arabidopsis S-phase kinase-related protein 1, TIMING OF CAB EXPRESSION 1, and PHYB. Interaction with PHYB was unaffected by mutation of any ZTL domain. Mutation of the kelch repeat domain affected protein binding at both the LOV/PAS and the F-box domains, indicating that interaction among ZTL domains leads to the strong phenotypes of kelch mutations. Forward genetics continues to provide insight regarding both known and newly discovered components of the circadian system, although current approaches have saturated mutations at some loci.},
	language = {English},
	number = {3},
	journal = {Plant Physiology},
	author = {Kevei, E. and Gyula, P. and Hall, A. and Kozma-Bognar, L. and Kim, W. Y. and Eriksson, M. E. and Toth, R. and Hanano, S. and Feher, B. and Southern, M. M. and Bastow, R. M. and Viczian, A. and Hibberd, V. and Davis, S. J. and Somers, D. E. and Nagy, F. and Millar, A. J.},
	month = mar,
	year = {2006},
	note = {Place: Rockville
Publisher: Amer Soc Plant Biologists
WOS:000235868900013},
	keywords = {arabidopsis-thaliana, degradation, encodes, flowering time, light, photoreceptors, phytochrome interacting factor-3, protein, rhythms, system},
	pages = {933--945},
}

2003 (1)

Changes in gene expression in the wood-forming tissue of transgenic hybrid aspen with increased secondary growth. Israelsson, M., Eriksson, M. E., Hertzberg, M., Aspeborg, H., Nilsson, P., & Moritz, T. Plant Molecular Biology, 52(4): 893–903. July 2003.

Changes in gene expression in the wood-forming tissue of transgenic hybrid aspen with increased secondary growth [link]

Paper doi link bibtex abstract

@article{israelsson_changes_2003,
	title = {Changes in gene expression in the wood-forming tissue of transgenic hybrid aspen with increased secondary growth},
	volume = {52},
	issn = {1573-5028},
	url = {https://doi.org/10.1023/A:1025097410445},
	doi = {10/b7zwj2},
	abstract = {Transgenic lines of hybrid aspen with elevated levels of gibberellin (GA) show greatly increased numbers of xylem fibres and increases in xylem fibre length. These plants therefore provide excellent models for studying secondary growth. We have used cDNA microarry analysis to investigate how gene transcription in the developing xylem is affected by GA-induced growth. A recent investigation has shown that genes encoding lignin and cellulose biosynthetic enzymes, as well as a number of transcription factors and other potential regulators of xylogenesis, are under developmental-stage-specific transcriptional control. The present study shows that the highest transcript changes in our transgenic trees occurs in genes generally restricted to the early stages of xylogenesis, including cell division, early expansion and late expansion. The results reveal genes among those arrayed that are up-regulated with an increased xylem production, thus indicating key components in the production of wood.},
	language = {en},
	number = {4},
	urldate = {2022-03-11},
	journal = {Plant Molecular Biology},
	author = {Israelsson, Maria and Eriksson, Maria E. and Hertzberg, Magnus and Aspeborg, Henrik and Nilsson, Peter and Moritz, Thomas},
	month = jul,
	year = {2003},
	pages = {893--903},
}

2002 (1)

Daylength and spatial expression of a gibberellin 20-oxidase isolated from hybrid aspen (Populus tremula L. × P. tremuloides Michx.). Eriksson, M. E., & Moritz, T. Planta, 214(6): 920–930. April 2002.

Daylength and spatial expression of a gibberellin 20-oxidase isolated from hybrid aspen (Populus tremula L. × P. tremuloides Michx.) [link]

Paper doi link bibtex abstract

@article{eriksson_daylength_2002,
	title = {Daylength and spatial expression of a gibberellin 20-oxidase isolated from hybrid aspen ({Populus} tremula {L}. × {P}. tremuloides {Michx}.)},
	volume = {214},
	issn = {1432-2048},
	url = {https://doi.org/10.1007/s00425-001-0703-3},
	doi = {10/bn4z3p},
	abstract = {Physiologically active gibberellins (GAs) are key regulators of shoot growth in trees. To investigate this mechanism of GA-controlled growth in hybrid aspen, we cloned cDNAs encoding gibberellin 20-oxidase (GA 20-oxidase), a key, highly regulated enzyme in the biosynthesis of GAs. Clones were isolated from leaf and cambium cDNA libraries using probes generated by polymerase chain reaction, based on conserved domains of GA 20-oxidases. Upon expression in Escherichia coli, the GST-fusion protein was shown to oxidise GA12 as well as oxidising the 13-hydroxylated substrate GA53, successively to GA9 and GA20, respectively. The gene PttGA20ox1 was expressed in meristematic cells and growing tissues such as expanding internodes, leaves and roots. The expression was negatively regulated by both GA4 and overexpression of phytochrome A. RNA analysis also showed that the expression was down-regulated in late-expanding leaf tissue in response to short days (SDs). Actively growing tissues such as early elongating internodes, petioles and leaf blades had the highest levels of C19-GAs. Upon transfer to SDs an accumulation of GA19 was observed in early elongating internodes and leaf blades. The levels of C19-GAs were also to some extent changed upon transfer to SDs. The levels of GA20 were down-regulated in internodes, and those of GA1 were significantly reduced in early expanding leaf blades. In roots the metabolites GA19 and GA8 decreased upon shifts to SDs, while GA20 accumulated slightly. The down-regulation of GA 20-oxidase activity in response to SDs was further indicated by studies of [14C]GA12 metabolism in shoots, demonstrating that the substrate for GA 20-oxidase, [14C]GA53, accumulates in SDs.},
	language = {en},
	number = {6},
	urldate = {2021-10-19},
	journal = {Planta},
	author = {Eriksson, Maria E. and Moritz, Thomas},
	month = apr,
	year = {2002},
	pages = {920--930},
}

2000 (1)

Increased gibberellin biosynthesis in transgenic trees promotes growth, biomass production and xylem fiber length. Eriksson, M. E., Israelsson, M., Olsson, O., & Moritz, T. Nature Biotechnology, 18(7): 784–788. July 2000. Bandiera_abtest: a Cg_type: Nature Research Journals Number: 7 Primary_atype: Research Publisher: Nature Publishing Group

Increased gibberellin biosynthesis in transgenic trees promotes growth, biomass production and xylem fiber length [link]

Paper doi link bibtex abstract

@article{eriksson_increased_2000,
	title = {Increased gibberellin biosynthesis in transgenic trees promotes growth, biomass production and xylem fiber length},
	volume = {18},
	copyright = {2000 Nature America Inc.},
	issn = {1546-1696},
	url = {https://www.nature.com/articles/nbt0700_784},
	doi = {10.1038/77355},
	abstract = {In most tree-breeding programs worldwide, increasing the trees' growth rates and stem volumes and shortening their rotation times are important aims. Such trees would yield more biomass per unit area. Here we show that overexpressing a key regulatory gene in the biosynthesis of the plant hormone gibberellin (GA) in hybrid aspen (Populus tremula × P. tremuloides) improves growth rate and biomass. In addition, these transgenic trees have more numerous and longer xylem fibers than unmodified wild-type (wt) plants. Long fibers are desirable in the production of strong paper, but it has not as yet proved possible to influence this trait by traditional breeding techniques. We also show that GA has an antagonistic effect on root initiation, as the transgenic lines showed poorer rooting than the control plants when potted in soil. However, the negative effect on rooting efficiencies in the initial establishment of young plantlets in the growth chamber did not significantly affect root growth at later stages.},
	language = {en},
	number = {7},
	urldate = {2021-11-08},
	journal = {Nature Biotechnology},
	author = {Eriksson, Maria E. and Israelsson, Maria and Olsson, Olof and Moritz, Thomas},
	month = jul,
	year = {2000},
	note = {Bandiera\_abtest: a
Cg\_type: Nature Research Journals
Number: 7
Primary\_atype: Research
Publisher: Nature Publishing Group},
	keywords = {Agriculture, Bioinformatics, Biomedical Engineering/Biotechnology, Biomedicine, Biotechnology, Life Sciences, general},
	pages = {784--788},
}

1997 (1)

Ectopic expression of oat phytochrome A in hybrid aspen changes critical daylength for growth and prevents cold acclimatization. Olsen, J. E., Junttila, O., Nilsen, J., Eriksson, M. E., Martinussen, I., Olsson, O., Sandberg, G., & Moritz, T. The Plant Journal, 12(6): 1339–1350. 1997. _eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1046/j.1365-313x.1997.12061339.x

Ectopic expression of oat phytochrome A in hybrid aspen changes critical daylength for growth and prevents cold acclimatization [link]

Paper doi link bibtex abstract

@article{olsen_ectopic_1997,
	title = {Ectopic expression of oat phytochrome {A} in hybrid aspen changes critical daylength for growth and prevents cold acclimatization},
	volume = {12},
	issn = {1365-313X},
	url = {https://onlinelibrary.wiley.com/doi/abs/10.1046/j.1365-313x.1997.12061339.x},
	doi = {10/c5z6sf},
	abstract = {Survival of temperate-zone tree species under the normal summer-winter cycle is dependent on proper timing of apical growth cessation and cold acclimatization. This timing is primarily based on the perception of daylength, and through evolution many tree species have developed photoperiodic ecotypes which are closely adapted to the local light conditions. The longest photoperiod inducing growth cessation, the critical photoperiod, is inherited as a quantitative character. The phytochrome pigment family is the probable receptor of daylength, but the exact role of phytochrome and the physiological basis for the different responses between photoperiodic ecotypes are not known. This report shows for the first time that over-expression of the oat phytochrome A gene (PHYA) in a tree significantly changes the critical daylength and effectively prevents cold acclimatization. While the critical daylength for elongation growth in the wild-type of hybrid aspen (Populus tremula × tremuloides) was approximately 15 h, transgenic lines with a strong expression of the oat PHYA gene did not stop growing even under a photoperiod of 6 h. Quantitative analysis of gibberellins (GA) as well as indole-3-acetic acid (IAA) revealed that levels of these were not down-regulated under short days in the transgenic plants expressing high levels of oat PHYA, as in the wild-type. These results indicate that photoperiodic responses in trees might be regulated by the amount of PHYA gene expressed in the plants, and that the amount of phytochrome A (phyA) affects the metabolism of GAs and IAA.},
	language = {en},
	number = {6},
	urldate = {2022-03-11},
	journal = {The Plant Journal},
	author = {Olsen, Jorunn E. and Junttila, Olavi and Nilsen, Jarle and Eriksson, Maria E. and Martinussen, Inger and Olsson, Olof and Sandberg, Göran and Moritz, Thomas},
	year = {1997},
	note = {\_eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1046/j.1365-313x.1997.12061339.x},
	pages = {1339--1350},
}